The effect of perinatal exposure to ethinyl oestradiol or a mixture of endocrine disrupting pesticides on kisspeptin neurons in the rat hypothalamus

NeuroToxicology

Volumn 37, Issue , 2013, Pages 154-162

  Overgaard, Agnete ^a   Holst, Klaus ^a,b   Mandrup, Karen R ^c   Boberg, Julie ^c   Christiansen, Sofie ^c   Jacobsen, Pernille R ^c   Hass, Ulla ^c   Mikkelsen, Jens D ^a  

^a University of Copenhagen   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Endocrine disruptors; Estrogen; Hypothalamus; Kiss1; Kisspeptin; Pesticides

Indexed keywords

ENDOCRINE DISRUPTOR; EPOXICONAZOLE; ETHINYLESTRADIOL; KISSPEPTIN; MANCOZEB; MESSENGER RNA; PROCHLORAZ; PROCYMIDONE; SEX HORMONE; TEBUCONAZOLE; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTEROVENTRAL PERIVENTRICULAR NUCLEUS; ARCUATE NUCLEUS; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HYPOTHALAMUS; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IN SITU HYBRIDIZATION; KISS1 GENE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL DRUG EXPOSURE; PRIORITY JOURNAL; PUBERTY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCRINE DISRUPTORS; ETHINYL ESTRADIOL; FEMALE; HYPOTHALAMUS; KISSPEPTINS; MALE; NEURONS; PESTICIDES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RNA, MESSENGER; SEXUAL MATURATION;

RATTUS;

EID: 84878849003     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2013.04.012     Document Type: Article

References (66)

1. Axelstad M., Boberg J., Nellemann C., Kiersgaard M., Jacobsen P.R., Christiansen S., et al. Exposure to the widely used fungicide mancozeb causes thyroid hormone disruption in rat dams but no behavioral effects in the offspring. Toxicol Sci 2011, 120:439-446.
2. Bakker J., Brock O. Early oestrogens in shaping reproductive networks: evidence for a potential organisational role of oestradiol in female brain development. J Neuroendocrinol 2010, 22:728-735.
3. Bateman H.L., Patisaul H.B. Disrupted female reproductive physiology following neonatal exposure to phytoestrogens or estrogen specific ligands is associated with decreased GnRH activation and kisspeptin fiber density in the hypothalamus. Neurotoxicology 2008, 29:988-997.
4. Bellingham M., Fowler P.A., Amezaga M.R., Rhind S.M., Cotinot C., Mandon-Pepin B., et al. Exposure to a complex cocktail of environmental endocrine-disrupting compounds disturbs the kisspeptin/GPR54 system in ovine hypothalamus and pituitary gland. Environ Health Perspect 2009, 117:1556-1562.
5. Benedetto A., Au C., Avila D.S., Milatovic D., Aschner M. Extracellular dopamine potentiates mn-induced oxidative stress, lifespan reduction, and dopaminergic neurodegeneration in a BLI-3-dependent manner in Caenorhabditis elegans. PLoS Genet 2010, 6(8):e1001084.
6. Bentsen A.H., Ansel L., Simonneaux V., Tena-Sempere M., Juul A., Mikkelsen J.D. Maturation of kisspeptinergic neurons coincides with puberty onset in male rats. Peptides 2010, 31:275-283.
7. Birkhøj M., Nellemann C., Jarfelt K., Jacobsen H., Andersen H.R., Dalgaard M., et al. The combined antiandrogenic effects of five commonly used pesticides. Toxicol Appl Pharmacol 2004, 201:10-20.
8. Buck Louis G.M., Gray L.E., Marcus M., Ojeda S.R., Pescovitz O.H., Witchel S.F., et al. Environmental factors and puberty timing: expert panel research needs. Pediatrics 2008, 121(Suppl 3):S192-S207.
9. Christian M., Gillies G. Developing hypothalamic dopaminergic neurones as potential targets for environmental estrogens. J Endocrinol 1999, 160:R1-R6.
10. Christiansen S., Scholze M., Dalgaard M., Vinggaard A.M., Axelstad M., Kortenkamp A., et al. Synergistic disruption of external male sex organ development by a mixture of four antiandrogens. Environ Health Perspect 2009, 117:1839-1846.
11. Clarkson J., Boon W.C., Simpson E.R., Herbison A.E. Postnatal development of an estradiol-kisspeptin positive feedback mechanism implicated in puberty onset. Endocrinology 2009, 150:3214-3220.
12. Clarkson J., Shamas S., Mallinson S., Herbison A.E. Gonadal steroid induction of kisspeptin peptide expression in the rostral periventricular area of the third ventricle during postnatal development in the male mouse. J Neuroendocrinol 2012, 24(6):907-915.
13. Cooper R.L., Laws S.C., Das P.C., Narotsky M.G., Goldman J.M., Tyrey E.L., et al. Atrazine and reproductive function: mode and mechanism of action studies. Birth Defects Res B Dev Reprod Toxicol 2007, 80:98-112.
14. Crain D.A., Janssen S.J., Edwards T.M., Heindel J., Ho S.M., Hunt P., et al. Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil Steril 2008, 90:911-940.
15. Davis L.K., Murr A.S., Best D.S., Fraites M.J., Zorrilla L.M., Narotsky M.G., et al. The effects of prenatal exposure to atrazine on pubertal and postnatal reproductive indices in the female rat. Reprod Toxicol 2011, 32:43-51.
16. de Roux N., Genin E., Carel J.C., Matsuda F., Chaussain J.L., Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proceedings of the National Academy of Sciences of the United States of America 100: 2003, 10972-10976.
17. Dickerson S.M., Cunningham S.L., Patisaul H.B., Woller M.J., Gore A.C. Endocrine disruption of brain sexual differentiation by developmental PCB exposure. Endocrinology 2011, 152:581-594.
18. Euling S.Y., Selevan S.G., Pescovitz O.H., Skakkebaek N.E. Role of environmental factors in the timing of puberty. Pediatrics 2008, 121(Suppl 3):S167-S171.
19. Frye C.A., Bo E., Calamandrei G., Calza L., Dessi-Fulgheri F., Fernandez M., et al. Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J Neuroendocrinol 2012, 24:144-159.
20. Goodman R.L., Maltby M.J., Millar R.P., Hileman S.M., Nestor C.C., Whited B., et al. Evidence that dopamine acts via kisspeptin to hold GnRH pulse frequency in check in anestrous ewes. Endocrinology 2012, 153:5918-5927.
21. Harrison Brody A., Chou E., Gray J.M., Pokyrwka N.J., Raley-Susman K.M. Mancozeb-induced behavioral deficits precede structural neural degeneration. Neurotoxicology 2013, 34:74-81.
22. Hass U., Boberg J., Christiansen S., Jacobsen P.R., Vinggaard A.M., Taxvig C., et al. Adverse effects on sexual development in rat offspring after low dose exposure to a mixture of endocrine disrupting pesticides. Reprod Toxicol 2012, 34(2):261-274.
23. Hurley P.M. Mode of carcinogenic action of pesticides inducing thyroid follicular cell tumors in rodents. Environ Health Perspect 1998, 106:437-445.
24. Jacobsen P.R., Christiansen S., Boberg J., Nellemann C., Hass U. Combined exposure to endocrine disrupting pesticides impairs parturition, causes pup mortality and affects sexual differentiation in rats. Int J Androl 2010, 33:434-442.
25. Jacobsen P.R., Axelstad M., Boberg J., Isling L.K., Christiansen S., Mandrup K.R., et al. Persistent developmental toxicity in rat offspring after low dose exposure to a mixture of endocrine disrupting pesticides. Reprod Toxicol 2012, 34(2):237-250.
26. Janner M., Fluck C.E., Mullis P.E. Impact of estrogen replacement throughout childhood on growth, pituitary-gonadal axis and bone in a 46,XX patient with CYP19A1 deficiency. Horm Res Paediatr 2012, 78:261-268.
27. Kamel F., Tanner C., Umbach D., Hoppin J., Alavanja M., Blair A., et al. Pesticide exposure and self-reported Parkinson's disease in the agricultural health study. Am J Epidemiol 2007, 165:364-374.
28. Kauffman A.S., Gottsch M.L., Roa J., Byquist A.C., Crown A., Clifton D.K., et al. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 2007, 148:1774-1783.
29. Kauffman A.S., Navarro V.M., Kim J., Clifton D.K., Steiner R.A. Sex differences in the regulation of Kiss1/NKB neurons in juvenile mice: implications for the timing of puberty. Am J Physiol Endocrinol Metab 2009, 297:E1212-E1221.
30. Kjaerstad M.B., Taxvig C., Andersen H.R., Nellemann C. Mixture effects of endocrine disrupting compounds in vitro. Int J Androl 2010, 33:425-433.
31. Kjaerstad M.B., Taxvig C., Nellemann C., Vinggaard A.M., Andersen H.R. Endocrine disrupting effects in vitro of conazole antifungals used as pesticides and pharmaceuticals. Reprod Toxicol 2010, 30:573-582.
32. Larsen P.J., Mikkelsen J.D., Jessop D.S., Lightman S.L., Chowdrey H.S. Neuropeptide Y mRNA and immunoreactivity in hypothalamic neuroendocrine neurons: effects of adrenalectomy and chronic osmotic stimulation. J Neurosci 1993, 13:1138-1147.
33. Laws S.C., Ferrell J.M., Stoker T.E., Schmid J., Cooper R.L. The effects of atrazine on female wistar rats: an evaluation of the protocol for assessing pubertal development and thyroid function. Toxicol Sci 2000, 58:366-376.
34. Lehman M.N., Merkley C.M., Coolen L.M., Goodman R.L. Anatomy of the kisspeptin neural network in mammals. Brain Res 2010, 1364:90-102.
35. Losa-Ward S.M., Todd K.L., McCaffrey K.A., Tsutsui K., Patisaul H.B. Disrupted organization of RFamide pathways in the hypothalamus is associated with advanced puberty in female rats neonatally exposed to bisphenol A. Biol Reprod 2012, 87(2):1-9.
36. Mandrup K.R., Hass U., Christiansen S., Boberg J. Perinatal ethinyl oestradiol alters mammary gland development in male and female Wistar rats. Int J Androl 2012, 35:385-396.
37. Mandrup K.R., Jacobsen P.R., Isling L.K., Axelstad A., Dreisig K., Hadrup N., et al. Effects of perinatal ethinyl estradiol exposure in male and female Wistar rats. Reprod Toxicol 2013, Under review with.
38. Marty M.S., Crissman J.W., Carney E.W. Evaluation of the EDSTAC female pubertal assay in CD rats using 17beta-estradiol, steroid biosynthesis inhibitors, and a thyroid inhibitor. Toxicol Sci 1999, 52:269-277.
39. Mayer C., Acosta-Martinez M., Dubois S.L., Wolfe A., Radovick S., Boehm U., et al. Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proc Natl Acad Sci U S A 2010, 107:22693-22698.
40. Mouritsen A., Aksglaede L., Sorensen K., Mogensen S.S., Leffers H., Main K.M., et al. Hypothesis: exposure to endocrine-disrupting chemicals may interfere with timing of puberty. Int J Androl 2010, 33:346-359.
41. Navarro V.M., Sanchez-Garrido M.A., Castellano J.M., Roa J., Garcia-Galiano D., Pineda R., et al. Persistent impairment of hypothalamic KiSS-1 system after exposures to estrogenic compounds at critical periods of brain sex differentiation. Endocrinology 2009, 150:2359-2367.
42. Orton F., Rosivatz E., Scholze M., Kortenkamp A. Widely used pesticides with previously unknown endocrine activity revealed as in vitro antiandrogens. Environ Health Perspect 2011, 119:794-800.
43. Ostby J., Kelce W.R., Lambright C., Wolf C.J., Mann P., Gray L.E. The fungicide procymidone alters sexual differentiation in the male rat by acting as an androgen-receptor antagonist in vivo and in vitro. Toxicol Ind Health 1999, 15:80-93.
44. Patisaul H.B., Adewale H.B. Long-term effects of environmental endocrine disruptors on reproductive physiology and behavior. Front Behav Neurosci 2009, 3:10.
45. Patisaul H.B., Todd K.L., Mickens J.A., Adewale H.B. Impact of neonatal exposure to the ERalpha agonist PPT, bisphenol-A or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats. Neurotoxicology 2009, 30:350-357.
46. Pinilla L., Aguilar E., Dieguez C., Millar R.P., Tena-Sempere M. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev 2012, 92:1235-1316.
47. Rajapakse N., Silva E., Kortenkamp A. Combining xenoestrogens at levels below individual no-observed-effect concentrations dramatically enhances steroid hormone action. Environ Health Perspect 2002, 110:917-921.
48. Rasier G., Parent A.S., Gerard A., Lebrethon M.C., Bourguignon J.P. Early maturation of gonadotropin-releasing hormone secretion and sexual precocity after exposure of infant female rats to estradiol or dichlorodiphenyltrichloroethane. Biol Reprod 2007, 77:734-742.
49. Regulation(EC)No. 396/2005. Regulation (EC) No 396/2005 of the European Parliament and of the Council of 23 February 2005 on maximum residue levels of pesticides in or on food and feed of plant and animal origin and amending Council Directive 91/414/EEC ed. E Parliament.
50. Ribeiro A.C., Pfaff D.W., Devidze N. Estradiol modulates behavioral arousal and induces changes in gene expression profiles in brain regions involved in the control of vigilance. Eur J Neurosci 2009, 29:795-801.
51. Rider C.V., Furr J., Wilson V.S., Gray L.E. A mixture of seven antiandrogens induces reproductive malformations in rats. Int J Androl 2008, 31:249-262.
52. Roa J., Aguilar E., Dieguez C., Pinilla L., Tena-Sempere M. New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Front Neuroendocrinol 2008, 29:48-69.
53. Ross J.L., Quigley C.A., Cao D., Feuillan P., Kowal K., Chipmann J.J., et al. Growth hormone plus childhood low-dose estrogen in Turner's syndrome. N Engl J Med 2011, 364:1230-1242.
54. Ryan B.C., Hotchkiss A.K., Crofton K.M., Gray L.E. In utero and lactational exposure to bisphenol A, in contrast to ethinyl estradiol, does not alter sexually dimorphic behavior, puberty, fertility, and anatomy of female LE rats. Toxicol Sci 2010, 114(1):133-148.
55. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1108.
56. Semaan S.J., Kauffman A.S. Sexual differentiation and development of forebrain reproductive circuits. Curr Opin Neurobiol 2010, 20:424-431.
57. Seminara S.B., Messager S., Chatzidaki E.E., Thresher R.R., Acierno J.S., Shagoury J.K., et al. The GPR54 gene as a regulator of puberty. N Engl J Med 2003, 349:1614-1627.
58. Smith J.T., Cunningham M.J., Rissman E.F., Clifton D.K., Steiner R.A. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005, 146:3686-3692.
59. Smith J.T., Dungan H.M., Stoll E.A., Gottsch M.L., Braun R.E., Eacker S.M., et al. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 2005, 146:2976-2984.
60. Sorensen K., Mouritsen A., Aksglaede L., Hagen C.P., Mogensen S.S., Juul A. Recent secular trends in pubertal timing: implications for evaluation and diagnosis of precocious puberty. Horm Res Paediatr 2012, 77:137-145.
61. Stanko J.P., Enoch R.R., Rayner J.L., Davis C.C., Wolf D.C., Malarkey D.E., et al. Effects of prenatal exposure to a low dose atrazine metabolite mixture on pubertal timing and prostate development of male Long-Evans rats. Reprod Toxicol 2010, 30:540-549.
62. Taxvig C., Hass U., Axelstad M., Dalgaard M., Boberg J., Andreasen H.R., et al. Endocrine-disrupting activities in vivo of the fungicides tebuconazole and epoxiconazole. Toxicol Sci 2007, 100:464-473.
63. Vinggaard A.M., Nellemann C., Dalgaard M., Jorgensen E.B., Andersen H.R. Antiandrogenic effects in vitro and in vivo of the fungicide prochloraz. Toxicol Sci 2002, 69:344-353.
64. Vinggaard A.M., Christiansen S., Laier P., Poulsen M.E., Breinholt V., Jarfelt K., et al. Perinatal exposure to the fungicide prochloraz feminizes the male rat offspring. Toxicol Sci 2005, 85:886-897.
65. Weidner I.S., Moller H., Jensen T.K., Skakkebaek N.E. Cryptorchidism and hypospadias in sons of gardeners and farmers. Environ Health Perspect 1998, 106:793-796.
66. Wohlfahrt-Veje C., Andersen H.R., Schmidt I.M., Aksglaede L., Sorensen K., Juul A., et al. Early breast development in girls after prenatal exposure to non-persistent pesticides. Int J Androl 2012, 35(3):273-282.